Cryopreservation and cryoprotectors in protection of the swine sperm

Authors

  • Wildelfrancys Lima de Souza Laboratório de Reprodução Suína e Tecnologia de Sêmen da Faculdade de Veterinária da Universidade Estadual do Ceará
  • Lina Raquel Santos Araújo Laboratório de Reprodução Suína e Tecnologia de Sêmen da Faculdade de Veterinária da Universidade Estadual do Ceará
  • Ricardo Toniolli Laboratório de Reprodução Suína e Tecnologia de Sêmen da Faculdade de Veterinária da Universidade Estadual do Ceará

Keywords:

Boar, cyclodextrin, freezing, cryoprotectants

Abstract

The use of frozen semen presents lower conception rates and fewer piglets born per birth. This is due to the fact that cryopreservation causes variations in temperature, changes in sperm permeability and oxidative processes, and the swine semen naturally presents low antioxidant capacity and undergoes oxidative stress. However, several cryoprotectants are used for several species, and the use of cyclodextrin and amino acid-loaded cholesterol is already described, aiming to improve the semen after thawing. The addition of cholesterol to the semen prior to cryopreservation maintains the integrity of the acrosomal membrane and slows sperm capacitation, which can be facilitated by cyclodextrin loading. In parallel, research indicates the importance of the use of amino acids in the semen, which form a layer of thermal protection that preserves the integrity of the sperm cell, in addition to presenting osmorregulatory function. In this sense, the viability of the cryopreservation of the swine semen favors the genetic improvement, minimizes the transmission of pathogens and allows the formation of a germplasm bank. Therefore, it is necessary to improve the use of cryoprotectants in an ideal proportion, which maintains the integrity of the sperm membrane and does not detract from the sperm capacitation and acrosomal reaction required for fertilization.

References

AITKEN, R.J.; KRAUSZ, C. Oxidative stress, DNA damage and the Y chromosome. Reproduction, v.122, p.497-506, 2001.

ALVARENGA, M.A.; PAPA, F.O.; LANDIM-ALVARENGA, F.C.; MEDEIROS, A.S.L. Amides as cryoprotectants for freezing stallion semen: a review. Animal Reproduction Science, v.89, p.105-113, 2005.

ANDRADE, A.F.C.; PEDROSA, A.C.; PASSARELLI, M.S.; MARTINS, S.M.M.K. Protocolos e possibilidades de criopreservação de sêmen suíno. Revista Brasileira de Reprodução Animal, v.43, n.2, p.89-96, 2019.

ARAÚJO, L.R.S.; BARROS, T.B.; GUIMARÃES, D.B.; CANTANHÊDE, L.F.; DIAS, A.A.; TONIOLLI, R. Uso de diluentes e temperaturas alternativas na conservação prolongada do sêmen do varrão. Ciência Animal Brasileira, v.17, n.1, p.26-35, 2016.

ATTIA, Y.A.; EL-NAGGAR, A.S.; ABOU-SHEHEMA, B.M.; ABDELLA, A.A. Effect of Supplementation with Trimethylglycine (Betaine) and/or Vitamins on Semen Quality, Fertility, Antioxidant Status, DNA Repair and Welfare of Roosters Exposed to Chronic Heat Stress. Animals, v.9, p.1-15, 2019.

BENNERMANN, P.E.; BORTOLOZZO, F.P.; WENTZ, I.; CARDOSO, M.R.I. Motilidade espermática e integridade acrossomal em doses de sêmen suíno refrigeradas e inoculadas com Escherichia coli e Staphylococcus aureus. Ciência Rural, v.30, p.313-318, 2000.

BERGERON, A.; CRÊTE, M.H.; BRINDLE, Y.; MANJUNATH, P. Low-density lipoprotein fraction from hen`s egg yolk decreases the binding of the major protein of bovine seminal plasma to sperm and prevents lipid efflux from the sperm membrane. Biology of Reproduction, v.70, n.3, p.708-717, 2004.

BERNECIC, N.C.; ZHANG, M.; GADELLA, B.M.; BROUWERS, J.F.H.M.; JANSEN, J.W.A.; ARKESTEIJN, G.J.A.; GRAAF, S.P.; LEAHY, T. BODIPY-cholesterol can be reliably used to monitor cholesterol efflux from capacitating mammalian spermatozoa. Scientific Reports, v.9, p.1-12, 2019.

BOERKE, A.; TSAI, P.S.; GARCIA-GIL, N.; BREWIS, I.A.; GADELLA, B.M. Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction. Theriogenology, v.70, p.1188–1196, 2008.

BORTOLOZZO, F.P.; WENTZ, I.; BENNEMANN, P.E.; BERNARDI, M.L.; WOLLMANN, E.B.; FERREIRA, F.M.; BORCHARDT NETO, G. Inseminação artificial na suinocultura tecnificada. 1ª ed., Porto Alegre: Pallotti, 2005. 185p.

BUSTAMANTE, C.L.; SETCHELL, B.P. The uptake of amino acids, in particular Leucine, by isolated perfused testes of rats. Journal of Andrology, v.21, p.452-463, 2000.

CALDERAM, I.B.K.; MASCHIO, É.F.; MADEIRA, E.M.; ULGUIM, R.R.; RAMBO, G.; CORRÊA, É.K.; LUCIA JR, T.; DESCHAMPS, J.C.; CORRÊA, M.N. Inseminação artificial intra-uterina em leitoas com sêmen criopreservado com dimetilacetamida e glicerol. Ciência Rural, v.38, p.1978-1983, 2008.

CASTELO, T.S.; FROTA, T.R.; SILVA, A.R. Considerações sobre a criopreservação do sêmen de caprinos. Acta Veterinaria Brasilica, v.2, p.67-75, 2008.

CEROLINI, S.; MALDJIAN, A.; SURAI, P.; NOBLE, R. Viability, susceptibility to peroxidation and fatty acid composition of boar semen during liquid storage. Animal Reproduction Science, v.58, n.1-2, p.99–111, 2000.

CEROLINI, S.; MALDJIAN, A.; PIZZI, F.; GLIOZZI, T.M. Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction, v.121, p.395-401, 2001.

CHALLA, R.; AHUJA, A.; ALI, J.; KHAR, R.K. Cyclodextrins in drug delivery: an updated review. Journal of Pharmaceutical Science and Technology, v.6, supl.2, p.329-357, 2005.

CHUAYCHU-NOO, N.; THANANURAK, P.; CHANKITISAKUL, V.; VONGPRALU, T. Supplementing rooster sperm with Cholesterol-Loaded-Cyclodextrin improves fertility after cryopreservation. Cryobiology, v.74, p.8-12, 2017.

COLÉGIO BRASILEIRO DE REPRODUÇÃO ANIMAL (CBRA). Manual para Exame Andrológico e Avaliação de Sêmen Animal. 3a ed., Belo Horizonte: CBRA; 2013. 104p.

COOPER GM. The cell: a molecular approach. Washington: ASM Press, 1996. 673p.

CORCINI, C.D.; VARELA, A.S.; PIGOZZO, R.; RAMBO, G.; GOULARTE, K.L. Pre-freezing and post thawing quality of boar sperm for distinct portions of the ejaculate and as a function of protein bands present in seminal plasma. Livestock Science, v.145, n.1, p.28-33, 2012.

CÓRDOVA-IZQUIERDO, A.; OLIVA, J.H.; LLEÓ, B.; GARCÍA-ARTIGA, C.; CORCUERA, B.D.; PÉREZ-GUTIÉRREZ, J.F. Effect of diferente thawing temperatures on the viability, in vitro fertilizing capacity and chromatin condensation of frozen boar semen packaged in 5 mL straws. Animal Reproduction Science, v.92, p.145–154, 2006.

ÇOYAN, K.; BASPINAR, N.; BUCAK, M.N.; AKALIN, P.P; ATAMAN, M.B.; ÖMÜR, A.D.; GÜNGÖR, S.; KÜÇÜKGÜNAY, S.; ÖZKALP, B.; SARIÖZKAN, S. Influence of methionine and dithioerythritol on sperm motility, lipid peroxidation and antioxidant capacities during liquid storage of ram semen. Research in Veterinary Science. v.89, p.426–431, 2010.

DAVIS, B.K. Interaction of lipids with the plasma membrane of sperm cells. I. The antifertilization action of cholesterol. Archive of Andrology, v.5, p.249-254, 1980.

DAVOODIAN, N.; KADIVA, A.; AHMADI, E.; MOHEBBI, A. Effects of Two Amino Acids on Motion Parameters and Enzymatic Antioxidant Activity of Freeze-Thawed Stallion Spermatozoa. Journal of Equine Veterinary Science, v.59, p.49-56, 2017.

DZIEKOŃSKA, A., KINDER, M., FRASER, L., STRZEŻEK, J.; KORDAN, W. Metabolic activity of boar semen stored in different extenders supplemented with ostrich egg yolk lipoproteins. Journal of Veterinary Research, v.61, n.1, p.127-133, 2017.

EDDY, E.M.; O’BRIEN, D.A. The spermatozoon. In: KNOBIL, E.; NEIL, J.D. (Ed.). The Physiology of Reproduction. 2a ed., New York: Raven Press, p.29-77, 1994.

EL-SHESHTAWY, R.I.; EL-SISY, G.A.; EL-NATTAT, W.S. Use of selects aminoacids to improve buffalo bull semen cryopreservation. Global Veterinária, v.2, p.146-150, 2008.

FAGUNDES, B.; SILVA, J.F.S.; SHIMOYA, A.; CUNHA, I.C.N.; SOUZA, G.V.; TILBURG, M.F. Adição de alanina, glicina e glutamina ao meio crioprotetor seminal de garanhões Mangalarga Marchador. Revista Brasileira de Zootecnia, v.39, n.2, p.279-284, 2010.

FAHY, G.M. Analysis of “solution effects” injury. Equations for calculating phase diagram information of the ternary system NaCl-dimethylsulfoxide-water and NaCl-glycerol-water. Biophysical Journal, v.32, p.837-850, 1980.

FICKEL, J.; WAGENER, A.; LUDWIG, A. Semen cryopreservation and the conservation of endangered species. European Journal of Wildlife Research, v.53, p.81-89, 2007.

FLESCH, F.M.; GADELLA, B.M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochimica and Biophysica Acta, v.1469, p.197–235, 2000.

GUIMARÃES, D.B.; BARROS, T.B.; CANTANHÊDE, L.F. FEUGANG, J.M.; SOUZA, L.P.; TONIOLLI, R. Qualidade espermática durante a curva de resfriamento do sêmen suíno diluído em água de coco e pó visando sua criopreservação. Ciência Animal Brasileira, v.19, p.1-16, 2018.

HAMDI, S.M.; VIEITEZ, G.; JASPARD, B.; BARBARAS, R.; PERRET, B.; MIEUSSET, R.; PARINAUD, J.; COLLET, X. Effects of human follicular fluid and high-density lipoproteins on early spermatozoa hyperactivation and cholesterol efflux. Journal of Lipid Research, v.51, n.6, p.1363-1369, 2010.

HE, Y.; LI, D.; ZHANG, W.; TIAN, X.; PANG, W.; DU, R.; YANG, G.; YU, T. Boar sperm quality and oxidative status as affected by rosmarinic acid at 17 °C. Tropical Animal Health and Production, 2020. https://doi.org/10.1007/s11250-020-02246-1

HINTON, B.T. The testicular and epididymal luminal amino acids microenvironment in the rat. Journal of Andrology, v.11, p.498-505, 1990.

HIWASA, M.; KOHNO, H.; TOGARI, T.; OKABE, K.; FUKUI, Y. Fertility after different artificial insemination methods using a synthetic semen extender in sheep. Journal of Reproduction and Development, v.55, n.1, p.50-54, 2009.

HOLT, W.V.; MEDRANO, A.; THURSTON, L.M.; WATSON, P.F. The significance of cooling rates and animal variability for boar sperm cryopreservation: insights from the cryomicroscope. Theriogenology, v.63, n.2, p.370–382, 2005.

HOUPALATHI, R.; LÓPEZ-FANDIÑO, R.; ANTON, M. Bioactive egg compounds. 1a ed., New York: Springer Verlag, 2007. 296p.

JOHNSON, L.A.; WEITZE, K.F.; FISER, P.; MAXWELL, W.M. Storage of boar semen. Animal Reproduction Science, v.62, p.143-172, 2000.

KASHIWAZAKI, N.; OKUDA, Y.; SEITA, Y.; HISAMATSU, S.; SONOKI, S.; SHINO, M.; MASAOKA, T.; INOMATA, T. Comparison of glycerol, lactamide, acetamide and dimethylsulfoxide as cryoprotectants of Japanese White Rabbit spermatozoa. Journal of Reproduction and Development, v.52, p.511-516, 2006.

LADHA, S. Lipid heterogeneity and membrane fluidity in a highly polarized cell, the mammalian spermatozoon. The Journal of Membrane Biology, v.165, n.1, p.1-10, 1998.

LEE, Y.S.; LEE, S.; LEE, S.H.; YANG, B.K.; PARK, C.K. Effect of cholesterol-loaded-cyclodextrin on sperm viability and acrosome reaction in boar semen cryopreservation. Animal Reproduction Science, v.159, p.124-130, 2015.

LIMA, A.S., BITTENCOURT, R.F., RIBEIRO FILHO, A.L., LOIOLA, M.V.G., MENEZES, G.F.O., BARRETO, R.O., VASCONCELOS, I.C., SILVA, C.C., JESUS, E.O., SNOECK, P.P.N. Utilização da lipoproteína de baixa densidade, em diferentes concentrações, em meio diluidor para criopreservação do sêmen ovino. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, v.71, n.6, p.1889-1895, 2019.

LONE, S.A.; PRASAD, J.K.; GHOSH, S.K.; DAS, G.K.; BALAMURUGAN, B.; KATIYAR, R.; VERMA, M.R. Effect of incubation on freezability of cholesterol-loaded cyclodextrin treated buffalo (Bubalus bubalis) spermatozoa. Veterinary World, v.9, p.182-185, 2016.

LONE, S.A. Possible mechanisms of cholesterol-loaded cyclodextrin action on sperm during cryopreservation. Animal Reproduction Science, v.192, p.1-5, 2018.

LÓPEZ-SALGUERO, J.B.; FIERRO, R.; MICHALSKI, J.-C.; JIMÉNEZ-MORALES, I.; LEFEBVRE, T.; MONDRAGÓN-PAYNE, O.; BALDINI, S.F.; VERCOUTTER-EDOUART, A.-S.; GONZÁLEZ-MÁRQUEZ, H. Identification of lipid raft glycoproteins obtained from boar spermatozoa. Glycoconjugate Journal, 2020. https://doi.org/10.1007/s10719-020-09924-0

MARTINS-BESSA, A.; ROCHA, A.; MAYENCO-AGUIRRE, A. Incorporation of taurine and hypotaurine did not improve the efficiency of the Uppsala Equex II extender for dog semen freezing. Theriogenology, v.68, p.1088–1096, 2007.

MEDEIROS, C.M.O.; FORELL, F.; OLIVEIRA, A.T.D.; RODRIGUES, J.L. Current status of sperm cryopreservation: why isn't it better? Theriogenology, v.57, p.327-344, 2002.

MOCÉ, E.; BLANCH, E.; TOMÁS, C.; GRAHAM, J.K. Use of cholesterol in sperm cryopreservation: presente moment and perspectives to future. Reproduction in Domestic Animals, v.45, n.2, p.57-66, 2010a.

MOCÉ, E.; PURDY, P.H.; GRAHAM, J.K. Treating ram sperm with cholesterol-loaded cyclodextrins improves cryosurvival. Animal Reproduction Science, v.118, p.236–247, 2010b.

MORAES, E.A.; MATOS W.C.G.; GRAHAM, J.K.; FERRARI JUNIOR, W.D. Cholestanol-loaded-cyclodextrin improve the quality of stallion spermatozoa after cryopreservation. Animal Reproduction Science. v.158, p.19-24, 2015.

NEVES, M.M.; HENRY, M. Gema do ovo de galinha e a ação protetora de suas lipoproteínas de baixa densidade na criopreservação do sêmen: uma revisão. Revista Brasileira de Reprodução Animal, Belo Horizonte, v.36, n.4, p.209-214, 2012.

NIKOLOPOULOU, M.; SOUCEK, D.A.; VARY, J.C. Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochimica et Biophysica Acta, v.815, p.486–498, 1985.

NUNES, J.F. Inseminação artificial em caprinos. In: GONSALVEZ, P.B.D.; FIGUEIREDO, J.R.; FREITAS, V.J.F. Biotécnicas aplicadas à reprodução animal. São Paulo: Varela, 2002. p.111-125.

OLIVEIRA, E.C.S.; JULIANI, G.C.; MARQUES JR, A.P.; HENRY, M. In vitro evaluation of canine spermatozoa cryopreserved in different extenders. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, v.58, p.1116-1122, 2006.

PINART, E.; YESTE, M.; PRIETO-MARTÍNEZ, N.; REIXACH, J.; BONET, S. Sperm quality and fertility of boar seminal doses after 2 days of storage: Does the type of extender really matter? Theriogenology, v.83, p.1428–1437, 2015.

PRIETO‐MARTÍNEZ, N.; VILAGRAN, I.; MORATÓ, R.; ÁLAMO, M.M.R.; RODRÍGUEZ‐GIL, J.E.; BONET, S.; YESTE, .M. Relationship of aquaporins 3 (AQP3), 7 (AQP7), and 11 (AQP11) with boar sperm resilience to withstand freeze–thawing procedures. Andrology, v.5, n.6, p.1153-1164, 2017.

PURDY, P.H. A review on goat sperm cryopreservation. Small Ruminant Research, v.63, p.215-225, 2006.

PYLES, E. Criopreservação de embriões e oócitos. Bio Embryo; 2013. Acesso em 19 agosto de 2019. Disponível em: http://www.bioembryo.com.br/noticias.php?cat=1&subcat=2&id=188>

RAJORIYA, J.S.; PRASAD, J.K.; RAMTEKE, S.S.; PERUMAL, P.; GHOSH, S.K.; SINGH, M.; PANDE, M.; SRIVASTAVA, N. Enriching membrane cholesterol improves stability and cryosurvival of buffalo spermatozoa. Animal Reproduction Science, v.164, p.72-81, 2016.

RANA, A.P.; MAJUMDER, G.C.; MISRA, S.; GHOSH, A. Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochimica et Biophysica Acta, v.1061, p.185-196, 1991.

REJRAJI, H.; SION, B.; PRENSIER, G.; CARRERAS, M.; MOTTA, C.; FRENOUX, J.M.; VERICEL, E.; GRIZARD, G.; VERNET, P.; DREVET, J.R. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biology of Reproduction, v.74, p.1104-1113, 2006.

ROCHA, L.G.P.; ZANGERONIMO, M.G.; MURGAS, L.D.S.; OBERLENDER, G.; PEREIRA1, L.J.; PEREIRA, B.A.; CHAVES, B.R.; SILVA, D.M. Evaluation of two different boar semen freezing protocols and their effects on semen quality after thawing. Animal Reproduction, v.12, n.4, p.871-875, 2015.

RODRÍGUEZ-MARTÍNEZ, H. Laboratory semen assessment and prediction of fertility: still utopia? Reproduction in Domestics Animals, v.38, n.4, p.312-318, 2003.

RODRIGUES-MARTINEZ H, LARSSON B, PERTOFT H. Evaluation of sperm damage and techniques for sperm clean-up. Reproduction, Fertility and Development, v.9, p.297-308, 1997.

SAEZ, F.; OUVRIER, A.; DREVET, J.R. Epididymis cholesterol homeostasis and sperm fertilizing ability. Asian Journal of Andrology, v.13, p.11–17, 2011.

SALMON, V.M.; CASTONGUAY, F.; DEMERS-CARON, V.; LECLERC, P.; BAILEY, J.L. Cholesterol-loaded cyclodextrin improves ram sperm cryoresistance in skim milk-extender. Animal Reproduction Science, v.177, p.1-11, 2017.

SANCHEZ, S.A.; GUNTHER, G.; TRICERRI, M.A.; GRATTON, E. Methyl-bcyclodextrins preferentially remove cholesterol from the liquid disordered phase in giant unilamellar vesicles. Journal of Membrane Biology, v.241, p.1-10, 2011.

SANGEETA, S.; ARANGASAMY, A.; KULKARNI, S.; SELVARAJU, S. Role of amino acids as additives on sperm motility, plasma membrane integrity and lipid peroxidation levels at pre-freeze and post-thawed ram semen. Animal Reproduction Science, v.161, p.82-88, 2015.

SARAVIA, F, WALLGREN M, NAGY S, JOHANNISSON A, RODRÍGUEZ-MARTÍNEZ H. Deep freezing of concentrated boar semen for intrauterine insemination: effects on sperm viability. Theriogenology, v.63, n.5, p.1320–1333, 2005.

SARTORI, A.; BECHARA, E.J.H. Metilglioxal: uma toxina endógena? Química Nova, v.33, n.10, p.2193-2201, 2010.

SHI, J.; LI, Y.; REN, K.; XIE, Y.; YIN, W.; MO, Z. Characterization of cholesterol metabolism in Sertoli cells and spermatogenesis (Review). Molecular Medicine Reports, v.17, n.1, p.705-713, 2018.

SILVA, P.N.F.; GADELLA, B.M. Detection of damage in mammalian sperm cells. Theriogenology, v.65, p.958-978, 2006.

SNOECK, P.P.N. Aspectos da criopreservação de sêmen equino: composição do meio diluidor, curvas de congelação e fertilidade. 2003. 116p. Tese (Doutorado em Medicina Veterinária) – Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 2003.

SNOECK, P.P.N. Aspectos da criopreservação de sêmen equino: composição do meio diluidor, curvas de congelação e fertilidade. 2003. 116f. Tese (Doutorado em Medicina Veterinária) – Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 2003.

SOUZA, W.L.; MORAES, E.A.; COSTA, J.M.S; GRAHAM, J.K. Cholesterol-loaded cyclodextrin in fresh goat sperm improves cryosurvival rates. Revista Brasileira de Ciências Veterinárias, v.23, n.1/1, p.93-98, 2016.

SOUZA, W.L.; MORAES, E.A.; OLIVEIRA, R.P. Colesterol carregado pela ciclodextrina sobre a criopreservação dos espermatozoides de garanhões da raça Nordestina. Pesquisa Veterinária Brasileira, v.38, n.5, p.991-996, 2018.

TAVILANI, H.; GOODARZI, M.T.; DOOSTI, M.; VAISI-RAYGANI, A.; HASSANZADEH, T. Relationship between seminal antioxidant enzymes and the phospholipid and fatty acid composition of spermatozoa. Reproductive Biomedicine Online, v.16, n.5, p.649-656, 2008.

THOMAS, A.D.; MEYERS, S.A.; BALL, B.A. Capacitation-like changes in equine spermatozoa following cryopreservation. Theriogenology, v.65, p.1531-1550, 2006.

TONHATI, R. L-prolina no alívio do estresse térmico em tomateiro cultivado em ambiente protegido. 2018. 76p. Tese (Doutorado). 2018. DOI:10.11606/D.11.2019.tde-20032019-120556

TONIOLLI, R.; BARROS, T.B., TONIOLLI, L.S.2, GUIMARÃES, D.B., DIAS, A.V.; CANTANHÊDE, L.F.; ARAÚJO, L.R.S.; FILHO, I.B.Q. Qualidade espermática do ejaculado suíno conservado a 5 °C no diluente ACP-103® associado à gema de ovo. Ciência Animal v.23, n.2, p.45-57, 2013.

TONIOLLI, R.; GUIMARÃES, D.B.; BARROS, T.B. Proteínas do sêmen e sua relação com a resistência à congelação em ejaculados de diferentes varrões. Revista Brasileira de Reprodução Animal, v.41, p.297-311, 2017.

UGUR, M.R.; DINH, T.; HITIT, M.; KAYA, A.; TOPPER, E.; DIDION, B.; MEMILI, E. Amino acids of seminal Plasma associated with freezability of bull sperm. Frontiers in Cell and Developmental Biology, v.7, p.1-14, 2020.

VALENTE, S.S.; PEREIRA, R.M.; BAPTISTA, M.C. In vitro and in vivo fertility of ram semen cryopreserved in different extenders. Animal Reproduction Science, v.117, n.1-2, p.74-77, 2010.

VICENTE-CARRILLO, A., EKWALL, H., ÁLVAREZ-RODRÍGUEZ, M., RODRÍGUEZ-MARTÍNEZ, H. Membrane Stress During Thawing Elicits Redistribution of Aquaporin 7 But Not of Aquaporin 9 in Boar Spermatozoa. Reproduction in Domestic Animals, v.51, n5, p.665–679, 2016.

WABERSKI, D.; WEITZE, K.F.; GLEUMES, T.; SCHWARZ, M.; WILLMEN, T.; PETZOLDT, R. Effect of time of insemination relative to ovulation on fertility with liquid and frozen boar semen. Theriogenology, v.42, p.831-840, 1994.

WATSON, P.F. Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing functions. Reproduction, Fertility and Development, v.7, n.4, p.871-891, 1995.

WATSON, P.F. The causes of reduced fertility with cryopreserved semen. Animal Reproduction Science, v.60/61, p.481-492, 2000.

WONGTAWAN, T.; SARAVIA, F.; WALLGREN, M.; CABALLERO, I.; RODRIGUEZ- MARTINEZ, H. Fertility after deep intra-uterine artificial insemination of concentrated low-volume boar semen doses. Theriogenology, v.65, p.773–787, 2006.

YESTE, M. State-of-the-art of boar sperm preservation in liquid and frozen state. Animal Reproduction, v.14, n.1, p.69-81, 2017.

YESTE, M.; RODRÍGUEZ‐GIL, J.E.; BONET, S. Artificial insemination with frozen‐thawed boar sperm. Molecular Reproduction Development, v.84, n.9, p.802-813, 2017.

ZAJA, I.Z.; SAMARDZIJA, M.; VINCE, S.; VILIĆ, M.; MAJIĆ-BALIĆ, I.; DURICIĆ, D.; MILINKOVIĆ-TUR, S. Differences in seminal plasma and spermatozoa antioxidative systems and seminal plasma lipid and protein levels among boar breeds and hybrid genetic traits. Animal Reproduction Science, v.170, p.75-82, 2016.

Published

2022-11-10

How to Cite

SOUZA, W. L. de; ARAÚJO, L. R. S. .; TONIOLLI, R. . Cryopreservation and cryoprotectors in protection of the swine sperm. Ciência Animal, [S. l.], v. 31, n. 2, p. 76–92, 2022. Disponível em: https://revistas.uece.br/index.php/cienciaanimal/article/view/9359. Acesso em: 19 jul. 2024.